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Is humanlike cytoarchitectural asymmetry present in another species with complex social vocalization? A stereologic analysis of mustached bat auditory cortex.

Considerable evidence suggests that left hemispheric lateralization for language comprehension in humans is associated with cortical microstructural asymmetries. However, despite the fact that left hemispheric dominance for the analysis of species-specific social vocalizations has been reported in several other species, little is known concerning microstructural asymmetries in auditory cortex of nonhumans. To test whether such neuroanatomical lateralization characterizes another species with complex social vocalizations, we performed stereologic analyses of Nissl-stained cells in layer III of area DSCF in mustached bats (Pteronotus parnellii). Area DSCF was selected because it contains neurons which are sensitive to several temporal features of conspecific vocalizations. Primary visual cortex (V1) was also studied as a comparative reference. We measured neuron densities, glial densities, and neuronal volumes in both hemispheres of 10 adult male bats. Results indicate that these variables are not significantly lateralized in area DSCF or V1. Additionally, magnopyramidal cells (i.e., the largest 10% of neurons from both hemispheres) were not asymmetric in their frequency of distribution at the population level. Although several individual bats had asymmetric neuron distributions, consistent hemispheric bias was not evident. Absence of population-level microstructural asymmetry in area DSCF of mustached bats suggests alternative evolutionary scenarios including: (1) microstructural lateralization of auditory cortical circuitry may be a unique adaptation for human language, and (2) the specialized biosonar function of mustached bat auditory cortex may require symmetrical cytoarchitectural structure. Resolution of these alternatives will require further data on the microstructure of auditory cortex in species with lateralized perception of acoustic social communication.

Adaptation, Physiological↗

Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex.

Correlated neuronal activity is believed to play an important role in refining and maintaining cortical circuitry during early development. Here we provide evidence that globally and locally correlated activity mediate different forms of adult plasticity. Pulses of broad-spectrum noise were used to activate time-locked responses across large areas of the rat auditory cortex, globally synchronizing cortical activity. Brief tone pips were used to activate relatively small groups of neurons, generating locally correlated activity. Pairing pulsed noises with nucleus basalis (NB) stimulation in awake rats for 4 weeks broadened spectral tuning, disrupted tonotopic maps, and reduced spontaneous discharge correlation in the primary auditory cortex (AI), as examined under anesthesia. Those effects caused AI neurons to appear qualitatively similar to neurons in nonprimary auditory fields of naive animals. Subsequent pairing of tone pips with NB stimulation for a period of 4 weeks completely reversed these effects induced by previous noise-NB pairing. These findings further demonstrate that the adult auditory cortex retains a substantial capacity for receptive field plasticity and tonotopic map reorganization and that locally correlated activity plays an important role in plasticity in the adult, as in the developing cortex.

Acoustic Stimulation↗

Auditory cortex of the long-eared hedgehog (Hemiechinus auritus): II. Tuning properties.

The forebrain of hedgehogs is considered by many investigators as one of the simplest and most primitive among extant placental mammals. In a recent study we have shown that the auditory cortex of the long-eared hedgehog (Hemiechinus auritus) comprises two distinct auditory fields, which are tonotopically organized. In this study, we describe tuning properties of single cells in these two fields. Application of the Q10dB and Square Root measures for determining sharpness of tuning revealed that, although most of the cells in the more anterior field, which is considered primary, are sharply tuned, on the average they are more broadly tuned than cells in the primary auditory cortex of other mammals. In the posterior field, the distribution of narrowly and broadly tuned cells is equal. Narrowly tuned cells in both fields are equally narrow, as are the broadly tuned cells. Latencies of single cells in both fields are frequency and intensity dependent and are somewhat longer than these found in other mammals. The distribution of BFs vs. threshold intensity matches fairly well the behavioral audiogram previously described. Our findings suggest that, in spite of the view that the isocortex of hedgehogs represents a 'primitive' condition, some basic tuning properties of their auditory cortex cells are comparable to those of other mammals.

Animals↗

Functional fields in human auditory cortex revealed by time-resolved fMRI without interference of EPI noise.

The gradient switching during fast echoplanar functional magnetic resonance imaging (EPI-fMRI) produces loud noises that may interact with the functional activation of the central auditory system induced by experimental acoustic stimuli. This interaction is unpredictable and is likely to confound the interpretation of functional maps of the auditory cortex. In the present study we used an experimental design which does not require the presentation of stimuli during EPI acquisitions and allows for mapping of the auditory cortex without the interference of scanner noise. The design relies on the physiological delays between the onset, or the end, of stimulation and the corresponding hemodynamic response. Owing to these delays and through a time-resolved acquisition protocol it is possible to analyze the decay of the stimulus-specific signal changes after the cessation of the stimulus itself and before the onset of the EPI-acoustic noise related activation (decay-sampling technique). This experimental design, which might permit a more detailed insight in the auditory cortex, has been applied to the study of the cortical responses to pulsed 1000 Hz sine tones. Distinct activation clusters were detected in the Heschl's gyri and the planum temporale, with an increased extension compared to a conventional block-design paradigm. Furthermore, the comparison of the hemodynamic response of the most anterior and the posterior clusters of activation highlighted differential response patterns to the sound stimulation and to the EPI-noise. These differences, attributable to reciprocal saturation effects unevenly distributed over the superior temporal cortex, provided evidence for functionally distinct auditory fields.

Acoustic Stimulation↗

Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques.

1. The ability of four Japanese macaques (Macaca fuscata) to localize sound was determined after bilateral ablation of auditory cortex. The animals were given two tests: a "midline" test in which they had to discriminate noise bursts presented from a loudspeaker located to the left from identical noise bursts presented from a loudspeaker located to the right of midline, and a "hemifield" test in which both loudspeakers were located in their right hemifield. 2. Both of the tests were administered by the use of two different behavioral tasks: a conditioned-avoidance task in which the animals were trained to make or break contact with a water spout to indicate the location of a sound source, and a two-choice task that required the animals to walk to the source of the sound. 3. The results of both the conditioned-avoidance and the two-choice tasks demonstrated that the animals were able to perform the midline discrimination although their localization acuity was reduced. However, the animals had great difficulty in learning to walk to the source of a sound in spite of the fact that they had received previous sound-localization training in the conditioned-avoidance task. This difficulty suggested that the monkeys no longer associated the sound with a location in space. 4. The results of both the conditioned-avoidance and the two-choice tasks demonstrated that the animals were unable to discriminate the locus of a sound source when both loudspeakers were located in the same hemifield. 5. Bilateral ablation of auditory cortex results in both sensory and perceptual deficits. The presence of sensory deficits is indicated by the decreased acuity in the left-right discrimination and the inability to discriminate between two loudspeakers located in the same hemifield. The deficit in the perception of the locus of sound is indicated by the difficulty in learning to approach the source of a sound, an ability which normal monkeys exhibit without training. 6. There appear to be species' differences in the effect of auditory cortex lesions on sound localization. Although cortical lesions result in a sound-localization deficit in several species of primates and carnivores, they have little or no effect on rats.

Animals↗

Functional MR of the primary auditory cortex: an analysis of pure tone activation and tone discrimination.

PURPOSE: To use functional MR imaging to measure the effect of frequency (pitch), intensity (loudness), and complexity of auditory stimuli on activation in the primary and secondary auditory cortexes. METHODS: Multiplanar echo-planar images were acquired in healthy subjects with normal hearing to whom auditory stimuli were presented intermittently. Functional images were processed from the echo-planar images with conventional postprocessing methods. The stimuli included pure tones with a single frequency and intensity, pure tones with the frequency stepped between 1,000, 2,000, 3,000, or 4,000 Hz, and spoken text. The pixels activated by each task in the transverse temporal gyrus (TTG) and the auditory association areas were tabulated. RESULTS: The pure tone task activated the TTG. The 1,000-Hz tone activated significantly more pixels in the TTG than did the 4,000-Hz tone. The 4,000-Hz tone activated pixels primarily in the medial TTG, whereas the 1,000-Hz tone activated more pixels in the lateral TTG. Higher intensity tones activated significantly more pixels than did lower intensity tones at the same frequency. The stepped tones activated more pixels than the pure tones, but the difference was not significant. The text task produced significantly more activation than did the pure tones in the TTG and in the auditory association areas. The more complex tasks (stepped tones and listening to text) tended to activate more pixels in the left hemisphere than in the right, whereas the simpler tasks activated similar numbers of pixels in each hemisphere. CONCLUSION: Auditory stimuli activate the TTG and the association areas. Activation in the primary auditory cortex depends on frequency, intensity, and complexity of the auditory stimulus. Activation of the auditory association areas requires more complex auditory stimuli, such as the stepped tone task or text reading.

Acoustic Stimulation↗

From objective to subjective: pitch representation in the human auditory cortex.

Magnetic brain responses to infrequent changes in the pitch of complex sounds were recorded. The composition of the test sounds required that pitch-deviant stimuli elicited the mismatch response only if perceived pitch was represented in auditory sensory memory. Results revealed that subjective features, such as pitch, are formed from objective stimulus parameters (i.e. the spectral contents of a sound) before storing acoustic information in memory. The origin of the magnetic response to pitch change showed that pitch deviation was detected in the auditory cortex. Pitch memory might also be located in the auditory cortex, as previous evidence suggests that storage for an auditory feature lies in the vicinity of the neuronal elements activated by deviations in that feature.

Acoustic Stimulation↗

Sodium salicylate reduces inhibitory postsynaptic currents in neurons of rat auditory cortex.

Sodium salicylate (SS) is a medicine for anti-inflammation and for chronic pain relief with a side effect of tinnitus. To understand the cellular mechanisms of tinnitus induced by SS in the central auditory system, we examined effects of SS on evoked and miniature inhibitory postsynaptic currents (eIPSCs and mIPSCs) recorded from layer II/III pyramidal neurons of rat auditory cortex in a brain slice preparation with whole-cell patch-clamp techniques. Both eIPSCs and mIPSCs recorded from the auditory cortex could be completely blocked by bicuculline, a selective GABA(A) receptor antagonist. SS did not change the input resistance of neurons but was found to reversibly depress eIPSCs in a concentration-dependent manner. SS reduced eIPSCs to 82.3% of the control level at 0.5 mM (n=7) and to 60.9% at 1.4 mM (n=12). In addition, SS at 1.4 mM significantly reduced the amplitude of mIPSCs from 24.12+/-1.44 pA to 19.92+/-1.31 pA and reduced the frequency of mIPSCs from 1.34+/-0.23 Hz to 0.89+/-0.13 Hz (n=6). Our results demonstrate that SS attenuates inhibitory postsynaptic currents in the auditory cortex, suggesting that the alteration of inhibitory neural circuits may be one of the cellular mechanisms for tinnitus induced by SS in the central auditory region.

Animals↗

Functional MR imaging of the auditory cortex with electrical stimulation of the promontory in 35 deaf patients before cochlea implantation.

BACKGROUND AND PURPOSE: Promontory testing is used for preoperative assessment of the auditory pathway before cochlear implantation. This method depends on patient cooperation and cannot be used in children or disabled persons. Promontory stimulation during functional MR imaging (fMRI) provides a new and objective method to test the integrity of the auditory pathway. To evaluate the method, we performed this prospective study in deaf adult patients. METHODS: fMRI of the auditory pathway with electrical stimulation of the promontory was performed in 35 profoundly deaf patients, bilaterally in seven. For safe stimulation inside the MR environment, a specially designed nerve stimulator was used. We acquired nine sections parallel to the sylvian fissure by using an echo-planar pulse sequence (1.5 T). To evaluate the number of pixels in the auditory cortex, areas were counted and the minimum confidence level (p(st) value) was determined. The auditory pathway was called intact when the minimal p(st) value was 10(-5) or when the minimal p(st) value was 10(-4) in at least five activated pixels. RESULTS: Images in 85% of patients reporting an auditory sensation showed activation of the contralateral auditory cortex. In the group of patients reporting no hearing sensation, images in 75% did not show activation. CONCLUSION: This method can prove the intactness of the auditory pathway and help the surgeon in decision making before cochlear implantation. However, a negative finding should not be interpreted as indicating a nonfunctioning auditory pathway. Additional technical refinements and experience are needed to further improve this method.

Adult↗

Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunocytochemical localization of GABAergic neurons.

The goal of this study was to describe the development of gamma-aminobutyric acid (GABA)-containing neurons in visual and auditory cortex of ferrets. The laminar and tangential distribution of neurons containing excitatory, inhibitory, and neuromodulatory substances constrain the potential circuits which can form during development. Ferrets are born at an early stage of brain development, allowing examination of inhibitory circuit formation in cerebral cortex prior to thalamocortical ingrowth and cortical plate differentiation. Immunocytochemically labelled nonpyramidal GABA neurons were present from postnatal day 1 throughout development, in all cortical layers, and generally followed the inside-out pattern of neuronal migration into the cortical plate. Prior to postnatal day 14, pyramidal neurons with transient GABA immunoreactivity were also observed. The density of Nissl-stained and GABA-immunoreactive neurons was high early in development, declined markedly by postnatal day 20, then remained relatively constant until adulthood. However, examination of the proportion of GABA neurons revealed an unexpected late peak at postnatal day 60, then a decrease in adulthood. Visual and auditory cortex were similar in most respects, but the peak at postnatal day 60 and the final proportion of GABA neurons was higher in auditory cortex. The late peak suggests that inhibitory circuitry is stabilized relatively late in sensory cortical development, and thus that GABA neurons could provide an important substrate for experience-dependent plasticity at late stages of development.

Animals↗

Neural responses in primary auditory cortex mimic psychophysical, across-frequency-channel, gap-detection thresholds.

Responses of single- and multi-units in primary auditory cortex were recorded for gap-in-noise stimuli for different durations of the leading noise burst. Both firing rate and inter-spike interval representations were evaluated. The minimum detectable gap decreased in exponential fashion with the duration of the leading burst to reach an asymptote for durations of 100 ms. Despite the fact that leading and trailing noise bursts had the same frequency content, the dependence on leading burst duration was correlated with psychophysical estimates of across frequency channel (different frequency content of leading and trailing burst) gap thresholds in humans. The duration of the leading burst plus that of the gap was represented in the all-order inter-spike interval histograms for cortical neurons. The recovery functions for cortical neurons could be modeled on basis of fast synaptic depression and after-hyperpolarization produced by the onset response to the leading noise burst. This suggests that the minimum gap representation in the firing pattern of neurons in primary auditory cortex, and minimum gap detection in behavioral tasks is largely determined by properties intrinsic to those, or potentially subcortical, cells.

Acoustic Stimulation↗

[Role of the auditory cortex in animal recognition of synthesized vowels].

Discrimination of synthesized vowels [a] and [i] was studied in intact dogs and animals with an ablated auditory cortex. Electro-defensive and conditioned reflex methods were used. It has been found that as a result of learning an auditory image of a stationary vowel can be formed in intact dogs, which is invariant relatively to any change in the basic frequency of the voice, the intensity and duration of presentation (300 to 75 msec), and that two formants are sufficent for discrimination. The auditory image of the vowel is preserved after a bilateral ablation of the auditory cortical projection zone. Discrimination of vowels is disturbed in animals with a removed auditory cortex when information redundancy is reduced (diminished number of formants and reduced signal duration).

Animals↗

Multiple brain systems generating the rat auditory evoked potential. I. Characterization of the auditory cortex response.

The objectives of this study were to characterize the auditory cortex response in the rat and to examine its contributions to the auditory evoked potentials (AEPs) recorded from the dorsal and lateral skull. This was accomplished by simultaneously recording AEPs from the cortical surface and from skull screw electrodes in anesthetized animals. The initial positive-negative response (P17-N32) was largely restricted to the cortical region corresponding to area 41. More detailed examination of the AEP mapping revealed multiple subcomponents (P9, P14, P17, P19) underlying the initial positivity, with differing topographies. Stimulus-response properties further dissociated the multiple positive subcomponents. Reversible local neurochemical suppression confirmed the auditory cortical origin of these AEPs. The auditory cortex-generated AEPs were refractory to barbiturate anesthesia which eliminated all dorsal skull AEPs, indicating that primary auditory cortical AEPs do not make a significant contribution to the dorsal skull-recorded ('vertex') AEPs. The findings raise issues regarding multiple parallel auditory processing systems and their associated AEPs.

Acoustic Stimulation↗

Origin and immunolesioning of cholinergic basal forebrain innervation of cat primary auditory cortex.

Numerous studies have implicated the cholinergic basal forebrain (cBF) in the modulation of auditory cortical responses. This study aimed to accurately define the sources of cBF input to primary auditory cortex (AI) and to assess the efficacy of a cholinergic immunotoxin in cat. Three anaesthetized cats received multiple injections of horseradish-peroxidase conjugated wheatgerm-agglutin into physiologically identified AI. Following one to two days survival, tetramethylbenzidine histochemistry revealed the greatest number of retrogradely labeled cells in ipsilateral putamen, globus pallidus and internal capsule, and smaller numbers in more medial nuclei of the basal forebrain (BF). Concurrent choline acetyltransferase immunohistochemistry showed that almost 80% of the retrogradely labeled cells in BF were cholinergic, with the vast majority of these cells arising from the more lateral BF nuclei identified above. In the second part of the study, unilateral intraparenchymal injections of the cholinergic immunotoxin ME20.4-SAP were made into the putamen/globus pallidus nuclei of six cats. Immuno- and histochemistry revealed a massive reduction in the number of cholinergic cells in and around the targeted area, and a corresponding reduction in the density of cholinergic fibers in auditory cortex. These results are discussed in terms of their implications for investigations of the role of the cBF in cortical plasticity.

Acetylcholine↗

The representation of peripheral neural activity in the middle-latency evoked field of primary auditory cortex in humans(1).

Short sweeps with increasing instantaneous frequency (up-chirps) designed to compensate for the propagation delay along the human cochlea enhance the magnitude of wave V of the auditory brainstem responses, while time reversed sweeps (down-chirps) reduce the magnitude of wave V [Dau, T., Wegner, O., Mellert, V., Kollmeier, B., J. Acoust. Soc. Am. 107 (2000) 1530-1540]. This effect is due to synchronisation of frequency channels along the basilar membrane and it indicates that cochlear phase delays are preserved up to the input of the inferior colliculus. The present magnetoencephalography study was designed to investigate the influence of peripheral synchronisation on the activation in primary auditory cortex. Spatio-temporal source analysis of middle-latency auditory evoked fields (MAEFs) elicited by clicks and up- and down-chirps showed that up-chirps elicited significantly larger MAEF responses compared to clicks or down-chirps. Both N19m-P30m magnitude and its latency are influenced by peripheral cross-channel phase effects. Furthermore, deconvolution of the empirical source waveforms with spike probability functions simulated with a cochlear model indicated that the source waves for all stimulus conditions could be explained with the same unit-response function, i.e. a far field recorded cortical response of a very small cell assembly along the medio-lateral axis of Heschl's gyrus that receives input from a small number of excitatory fibres. The conclusion is that (i) phase delays between channels in the auditory pathway are preserved up to primary auditory cortex, and (ii) MAEFs can be described by a convolution of a unit-response function with the summary neural activity pattern of the auditory nerve.

Acoustic Stimulation↗

Sound frequency representation in cat auditory cortex.

Using the intrinsic signal optical recording technique, we reconstructed the two-dimensional pattern of stimulus-evoked neuronal activities in the auditory cortex of anesthetized and paralyzed cats. The average magnitude of intrinsic signal in response to a pure tone stimulus increased steadily as the sound pressure level increased. A detailed analysis demonstrated that the evoked signals at early frames were scaled by the sound pressure level, which in turn indicated the presence of a minimum level of sound pressure beyond which stimulus-related intrinsic signal can be generated. Intrinsic signals evoked significantly by pure tone stimuli of different frequencies were localized and arranged in an orderly manner in the middle ectosylvian gyrus, which indicates that the primary auditory field (AI) is tonotopically organized. The arrangement of optimal frequencies obtained from optical recordings of the same auditory cortex, which were conducted on different days, was highly reproducible. Furthermore, other auditory fields surrounding AI in the recorded area were allocated based on the observed tonotopicity. We also conducted unit recordings on the cats used for optical recording with the same set of acoustic stimuli. The gross feature of the arrangement of optimal frequencies determined by unit recordings agreed with the tonotopic arrangement determined by the optical recording, although the precise agreement was not obtained.

Acoustic Stimulation↗

[Reactions of neurons of the auditory cortex of unanesthetized cats to tones of a characteristic frequency].

Extra- and intracellular responses of primary auditory cortex (AI) neurons were studied in acute experiments on non-anaesthetized cats. It was found that auditory cortex neurons having similar best frequencies revealed various forms of responses to corresponding frequency tones. Neurons responded to the tone by on reactions constituted about 40% of nerve cells studied. 27% of neurons revealed responses of on-off and off types. 27% of cortical neurons responded by steady excitation or by inhibition of background activity. About 6% of neurons did not respond to the tone. During intracellular recordings about 85% of neurons studied responded to switching on and/or off of the tone by a spike-IPSP sequence. 96% of cortical neurons generated IPSP as a constant component of the response to tone. Tonic responses of auditory cortical neurons were the result of powerful and lasting depolarization of the postsynaptic membranes. The conclusion is made that interaction of excitatory and inhibitory processes is the most significant in any kind of responses of the auditory cortical neurons to tones.

Animals↗

Binaural processing of sound pressure level in cat primary auditory cortex: evidence for a representation based on absolute levels rather than interaural level differences.

1. Single-neuron responses were recorded in high-frequency regions of primary auditory cortex (AI) of anesthetized cats. Best-frequency tone pips were presented to each ear independently via sealed stimulus delivery systems, and the sound pressure level (SPL) at each ear was independently manipulated. Each neuron was studied with many dichotic combinations of SPL, chosen to incorporate a broad range of the two synthetic interaural level variables, interaural level difference (ILD) and average binaural level (ABL). This paper illustrates the common forms of binaural SPL selectivity observed in a sample of 204 single neurons located in AI. 2. Most neurons (> 90%) were jointly influenced by ILD and ABL. A small proportion of bilaterally excitable (EE) neurons responded to ABL rather independently of ILD. Only one neuron was determined to respond to ILD independently of ABL. 3. Nonmonotonic selectivity for one or both of the binaural level cues was evident in > 60% of our sample. Within the most effective range of ILD values, response strength was usually related nonmonotonically to related both to ILD and ABL. We have described units exhibiting this kind of dual nonmonotonic selectivity for the two binaural variables as being influenced by a Two-Way Intensity Network (TWIN). 4. Each of the response forms identified in an earlier study of the gerbil inferior colliculus were found in this study of cat auditory cortex. However the classes were evident in markedly different proportions. In particular, TWIN responses alone accounted for 36.2% of the sample, nearly four times the proportion found in the inferior colliculus in a previous study. 5. Units with similar binaural responses do not necessarily have similar monaural properties. For example, the typically nonmonotonic relation between response strength and ABL was often observed in the absence of a monaurally demonstrable nonmonotonicity. There is no simple relation between a neuron's classification according to the sign of monaural influence and its response to ILD and ABL. In particular, EE neurons exhibited remarkably diverse binaural properties. 6. Since responses of nearly all AI neurons are influenced jointly by ABL and ILD, we contend that single neurons in primary auditory cortex are not specifically tuned to either cue. ILD and ABL are mathematical expressions relating the SPLs at the two ears to each other (as the difference and average, respectively) and any such combination is expressed most simply as a particular combination of SPL at each ear.(ABSTRACT TRUNCATED AT 400 WORDS)

Acoustic Stimulation↗